Perceptual coupling and decoupling of the default mode network during mind-wandering and reading

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    Evaluation Summary:

    This manuscript is of broad interest to those interested in the relationship between mind wandering and reading, at the behavioral and neural levels, including when both processes occur at the same time. As such, this manuscript has important implications for clarifying how the experience of mind wandering while reading may occur. The results partially support the proposed theoretical framework that mind wandering during reading disrupts processing of visual input, however, not all of the authors' claims appear to be supported by the experimental design and data.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

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While reading, the mind can wander to unrelated autobiographical information, creating a perceptually-decoupled state detrimental to narrative comprehension. To understand how this mind-wandering state emerges, we asked whether retrieving autobiographical content necessitates functional disengagement from visual input. In Experiment 1, brain activity was recorded using functional magnetic resonance imaging (fMRI) in an experimental situation mimicking naturally occurring mind-wandering, allowing us to precisely delineate neural regions involved in memory and reading. Individuals read expository texts and ignored personally relevant autobiographical memories, as well as the opposite situation. Medial regions of the default mode network (DMN) were recruited during memory retrieval. In contrast, left temporal and lateral prefrontal regions of the DMN, as well as ventral visual cortex, were recruited when reading for comprehension. Experiment 2 used functional connectivity at rest to establish that (i) DMN regions linked to memory are more functionally decoupled from regions of ventral visual cortex than regions in the same network engaged when reading, and (ii) individuals reporting more mind-wandering and worse comprehension, while reading in the lab, showed increased functional decoupling between visually-connected DMN sites important for reading and a region of dorsal occipital cortex linked to autobiographical memory in Experiment 1. These data suggest we lose track of the narrative when our mind wanders because the generation of autobiographical mental content relies on cortical regions within the DMN which are functionally decoupled from ventral visual regions engaged during reading.

Significance statement

When the mind wanders during reading, we lose track of information from the narrative. We hypothesised that poor comprehension occurs because retrieving autobiographical memories reduces the perceptual coupling necessary to understand written words. We show that default mode network (DMN) areas involved in reading are functionally more connected to ventral visual regions than DMN regions important for autobiographical memory. Furthermore, individuals who mind-wander more, and comprehend less, have weaker connectivity between visually-coupled DMN regions linked to reading and dorsal occipital areas linked to autobiographical memory. These data suggest that when our minds wander during reading, retrieval of personally-relevant information activates DMN regions that are functionally disconnected from visual input, creating a perceptually decoupled state detrimental to comprehension.

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  1. Evaluation Summary:

    This manuscript is of broad interest to those interested in the relationship between mind wandering and reading, at the behavioral and neural levels, including when both processes occur at the same time. As such, this manuscript has important implications for clarifying how the experience of mind wandering while reading may occur. The results partially support the proposed theoretical framework that mind wandering during reading disrupts processing of visual input, however, not all of the authors' claims appear to be supported by the experimental design and data.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)

  2. Reviewer #1 (Public Review):

    The manuscript by Zhang et al. helps to establish the neural mechanisms underlying a well-established phenomenon in the cognitive literature on mind-wandering: mind-wandering while reading. This phenomenon is an interesting one because the brain's default mode network (DMN) has been proposed to support reading, as well as perceptually-decoupled thoughts such as autobiographical memories unrelated to reading that may underpin the experience of mind-wandering while reading. How the brain deals with these conflicting processes remains an open question. To examine this question, the authors designed a clever task in which some trials directed participants to focus on reading a sentence, while other trials asked participants to retrieve an autobiographical memory. Critically, in some of the trials, each of these "primary" tasks was accompanied by a distracting stimulus from the opposite domain (e.g. unrelated reading material when asked to retrieve an autobiographical memory and a distracting memory cue when asked to read expository text). The authors found that when the primary task was autobiographical memory retrieval, a set of DMN regions aligning with the DMN "core" and the DMN "medial temporal (MT) subsystem" became engaged to a greater degree than when the primary task was reading. Conversely, when the primary task was reading, there was greater involvement of regions overlapping with the "dorsal medial" DMN subsystem. Further, brain-behavior relationships show that increased involvement of the DMN core and MT subsystem during reading correlates with less perceived task focus. In Study 2, conducted in an independent sample of participants, regions recruited during reading in Study 1were more functionally coupled with ventral visual regions at rest than regions than regions recruited during autobiographical memory retrieval. Finally, individual difference analyses revealed that individuals who mind-wandered more while reading in a separate lab-based task exhibited decreased connectivity at rest between reading-related regions identified in Study 1 and a dorsal occipital region showing preferential involvement in autobiographical memory in the same study.

    Overall, these findings are important because they point to neuroanatomical differences between autobiographical memory and reading, and highlight a means by which autobiographical thoughts may pull one's primary attention away from reading, leading to impaired reading comprehension and memory. There are numerous strengths of this manuscript, including:


    1. Exploration of an important and pertinent topic. The topic explored by the authors bridges research on language, memory, and attention and will likely be of interest to a broad audience. Engaging in unrelated autobiographical thinking while reading may impair comprehension and memory for the reading material, and impairments in attention may be more pertinent in today's society given challenges to attention that have arisen from the COVID pandemic. Furthermore, heterogeneity of the DMN has been a matter of debate in recent years, which this study sheds light on.

    2. Largely converging findings across studies. The task-related results from Study 1 converge nicely with the resting state analyses from Study 2. The extension of the task-related findings to resting state and individual differences in behavior is a strength of the manuscript (although the individual difference analyses in Study 2 are a bit perplexing).

    3. The development of a clever set of tasks. It is logistically difficult to capture mind-wandering during reading in the scanner, so instead, the authors create a task which differentially emphasizes reading vs. autobiographical memory and include in these tasks distracting stimuli from the opposite task. Although I point out below that this task can also be seen as a "weakness" of the study because of its inability to fully capture the mind-wandering process, overall I think the authors do an excellent job given the difficulties of capturing an elusive process and the logistical issues with running the study in the MRI scanner.

    4. Clarity in conceptual organization and writing. The manuscript is very well written, well-motivated, and overall, a pleasure to read.

    5. A nice set of figures. The figures are clear, relevant and visually attractive.

    6. Sample size. The sample size in Study 1 (n=29) seems sufficient given the analyses performed, while the sample size in Studies 2 (n=244) and 3 (n=69) are sizeable.

    7. Manuscript data available for public use. The authors make their manuscript data available for public use, which promotes transparency and facilitates efforts toward reproducibility.

    However, in addition to the numerous strengths of this manuscript, there are also some notable weaknesses, including:


    1. Some of the authors' claims do not appear to be fully supported by the data presented. Most notably, there are likely many aspects of naturally-occurring mind-wandering during reading that may not be accurately captured by the autobiographical memory task. For example, naturally-emerging mind-wandering during reading is likely to be much more spontaneous in nature than the autobiographical memory task. The autobiographical memory task asks participants to deliberately recall and elaborate on a personal memory from the past related to a cue word. This is a deliberate, goal-directed process requiring participants to sustain attention to a mnemonic representation, which likely involves executive function resources. In contrast, autobiographical memories that occur while reading are more likely to occur spontaneously in nature. It is unclear how this fundamental difference influences the results and whether there are any discrepancies between brain regions highlighted during the autobiographical memory task and brain regions that may correspond to spontaneous memory recall during naturally-occurring reading.

    Relatedly, the phenomenological content of mind-wandering occasions during reading may be much broader than autobiographical memory. Participants may be distracted away from the reading by "external distractions," or they may engage in autobiographical or nonautobiographical thought pertaining to the future, the present, or non-temporal content. Indeed, the mind wandering content reports in Study 2 suggest that thoughts tend to only be somewhat past focused. Without measuring the variety of brain activity patterns as participants start to lose focus on the reading, the findings in the present manuscript are somewhat limited in scope to the role of autobiographical memory retrieval while reading, and may warrant more speculative conclusions considering the deliberate nature of the autobiographical memory task.

    Finally, the authors presented words serially in the naturalistic reading task and in short passages, yet naturalistic reading involves a self-paced process with longer length passages and a much more complex pattern of attentional focus on the text. One's natural pace of reading sometimes slows down or speeds up as one's attention, interest, or complexity waxes and wanes, and people also often re-read earlier parts of text, etc.. All of these differences point to an important discrepancy between the reading task and the natural reading which is not discussed as a possible limitation in the manuscript.

    1. The authors examined differences in fMRI activity during conflict reading trials as compared to "pure reading" trials, which would theoretically point to the role of automatically surfacing autobiographical memories acting as a source of distraction. Conflict reading trials are trials in which the primary task is to read, yet the participants are presented with a distracting autobiographical memory previously linked to an autobiographical memory in an earlier lab session. The behavioral data suggests that the autobiographical memory cue is indeed distracting to the reading process, suggesting it may facilitate autobiographical retrieval in more of an automatic way, possibly addressing the concern noted in comment #1. However, the fMRI contrast between reading with autobiographical memory conflict vs. pure reading did not yield any significant findings (data reported in Supplementary Information), raising some questions that the authors do not address in the discussion. Notably, the authors DO find that activity within the core and MT subsystems relates to less perceived task focus during the reading task, although the contrasts used in Figure 3C are unclear and I suspect don't focus on conflict > pure reading. These negative relationships are interesting, although it is surprising to me that the authors did not observe that the DM subsystem showed a positive relationship with task focus.

    2. The authors emphasize neural differences between autobiographical memory and reading, yet there may be neural similarities between the two processes that do not receive as much attention in the manuscript as I think should be warranted. The differences between autobiographical memory and reading emerged from a contrast showing brain regions with fMRI activity that is elevated to a greater degree for one task as compared to the other. It may well be that both autobiographical memory and reading recruit a more similar set of brain regions than highlighted by the difference analysis, yet do so to varying degrees. Indeed, prior research has emphasized the role of other regions in the DMN in reading and conceptual processing (e.g. Binder & Desai, 2011; Mar, 2011). Neural similarities between the processes seem important to emphasize, yet they may be difficult to fully test in this experiment because the baseline letter string control condition for reading and autobiographical memory is a passive task that may also recruit brain regions within the DMN due to the likelihood of mind-wandering.

    3. Along these lines, the authors could have more comprehensively discussed prior work linking narrative comprehension, conceptual processing, and reading to the DMN, including the dorsal medial PFC subsystem. Earlier and more recent meta-analyses seem important to incorporate here, and the link between reading and the dorsal medial PFC subsystem of the DMN (in particular) is also not a novel link in the literature.

    4. To me, the negative relationship between mind-wandering during laboratory reading tasks and connectivity with the dorsal occipital cortex region engaged during autobiographical memory seems to be the opposite direction to what I would have predicted given results from Study 1, raising questions that I would have liked to see be discussed in more detail in the discussion.

  3. Reviewer #2 (Public Review):

    The authors use three fMRI datasets (one with task data, n = 29, and two with rest, ns = 243 and 69) to test the hypothesis that mind wandering during reading disrupts the integration of visual input. In Experiment 1, they contrasted univariate activity observed while individuals read sentences one word at a time while ignoring a memory cue or retrieved autobiographical memories promoted by a memory cue while ignoring the sentences. Activity in lateral prefrontal default mode network (DMN) and visual regions was greater during reading, whereas activity in medial DMN regions was greater during memory retrieval. In Experiment 2 dataset 1, they showed that lateral DMN regions (linked to reading) are more strongly coupled with visual regions than are medial DMN regions (linked to memory) during rest. In Experiment 2 dataset 2, they relate individual differences in mind wandering to functional connectivity between lateral DMN regions (linked to reading) and a dorsal occipital region (linked to memory).

    Strengths of the paper include a rich theoretical motivation and framing, use of three independent fMRI datasets, complementary analyses of relationships between visual and DMN regions, and open data. Areas of potential improvement include demonstrating specificity of the observed results to mind wandering (rather than distraction from reading in general) and strengthening the evidence for replication across the three datasets.

    The reading comprehension and autobiographical memory task provides a unique opportunity to study the impact of off-task thought on reading in a controlled experimental setting. However, it leaves open the possibility that the same pattern of results would be observed in a reading task with any dual-task demand. It would be helpful to consider evidence about whether Experiment 1 findings are specific to reading disrupted by memory, or whether they reflect distraction from reading more generally.

    It is not readily apparent how precisely the findings agree across datasets because the brain regions described in each experiment and dataset partially but do not fully overlap, and it's not clear what degree of overlap should be considered a replication or what the likelihood of seeing that degree of overlap by chance would be.

    Finally, the manuscript frames mind wandering as detrimental to reading comprehension and operationalizes it as irrelevant to the text being read. For longer narratives than those used here, however, mind wandering could hypothetically facilitate comprehension. For example, imagine trying to recall clues in a mystery novel or an author's obscure literary reference. In this case would decoupling between DMN and sensory regions always impair comprehension and memory?